Differential activation of ammonium transporters during the accumulation of ammonia by Colletotrichum gloeosporioides and its effect on appressoria formation and pathogenicity

Molecular Plant-Microbe Interactions

Volumn 26, Issue 3, 2013, Pages 345-355

  Shnaiderman, Chen ^a,b   Miyara, Itay ^a   Kobiler, Ilana ^a   Sherman, Amir ^a   Prusky, Dov ^a  

^a VOLCANI CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; CARRIER PROTEIN; CYCLIC AMP; FUNGAL PROTEIN;

ARTICLE; COLLETOTRICHUM; FRUIT; FUNGUS SPORE; GENE DELETION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MYCELIUM; PATHOGENICITY; PERSEA; PH; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; TRANSPORT AT THE CELLULAR LEVEL; VIRULENCE;

AMMONIA; BIOLOGICAL TRANSPORT; COLLETOTRICHUM; CYCLIC AMP; FRUIT; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKOUT TECHNIQUES; HYDROGEN-ION CONCENTRATION; MEMBRANE TRANSPORT PROTEINS; MYCELIUM; PERSEA; PHENOTYPE; PLANT DISEASES; SEQUENCE DELETION; SPORES, FUNGAL; VIRULENCE;

EID: 84874072995     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-07-12-0170-R     Document Type: Article

References (53)

1. Adachi, K., and Hamer, J. E. 1998. Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grisea. Plant Cell 10:1361-1373.
2. Alkan, N., Fluhr, R., Sherman, A., and Prusky, D. 2008. Role of ammonia secretion and pH modulation on pathogenicity of Colletotrichum coccodes on tomato fruit. Mol. Plant-Microbe Interact. 21:1058-1066.
3. Alkan, N., Fluhr, R., Sagi, M., Davydov, O., and Prusky, D. 2009. Ammonia secreted by Colletotrichum coccodes affects host NADPH oxidase activity enhancing cell death and pathogenicity in tomato fruits. Mol. Plant-Microbe Interact. 22:1484-1491.
4. Alkan, N., Fluhr, R., and Prusky, D. 2012. Colletotrichum coccodes infection of ripe and unripe tomato fruit is modulated by ammonium secretion through salicylic and jasmonic acid pathways leading to PCD and differential colonization. Mol. Plant-Microbe Interact. 25:85-96.
5. Barad, S., Horowitz, S., Sherman, L., and Prusky, D. 2012. Penicillium expansum glucose oxidase-encoding gene, gox2, is essential for gluconic acid production and acidification during colonization of deciduous fruits. Mol. Plant-Microbe Interact. 25:779-788.
6. Barhoom, S., and Sharon, A. 2004. cAMP regulation of pathogenic and saprophytic fungal spore germination. Fungal Genet. Biol. 41:317-326.
7. Biswas, K., and Morschhäuser, J. 2005. The Mep2p ammonium permease controls nitrogen starvation-induced filamentous growth in Candida albicans. Mol. Microbiol. 56:649-669.
8. Brendon, J., Monahan, J., Fraser, J. A., Hynes, M. J., and Davis, M. A. 2002. Isolation and characterization of two ammonium permease genes, meaA and mepA, from Aspergillus nidulans. Eukaryot. Cell 1:85-94.
9. Choi, W. B., and Dean, R. A. 1997. The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9:1973-1983.
10. Davidzon, M., Alkan, N., Kobiler, I., and Prusky, D. 2010. Acidification by gluconic acid of mango fruit tissue during colonization via stem end infection by Phomopsis mangiferae. Postharvest Biol. Technol. 55:71-77.
11. Diéguez-Uribeondo, J., Förster, H., and Adaskaveg, J. E. 2008. Visualization of localized pathogen-induced pH modulation in almond tissues infected by Colletotrichum acutatum using confocal scanning laser microscopy. Phytopathology 98:1171-1178.
12. Drori, N., Kramer-Haimovich, H., Rollins, J., Dinoor, A., Okon, Y., Pines, O., and Prusky, D. 2003. A combination of external pH and nitrogen assimilation affects secretion of the virulence factor pectate lyase by Colletotrichum gloeosporioides. Appl. Environ. Microbiol. 69:3258-3262.
13. Eshel, D., Miyara, I., Ailinng, T., Dinoor, A., and Prusky, D. 2002. pH regulates endoglucanase expression and virulence of Alternaria alternata in persimmon fruits. Mol. Plant-Microbe Interact. 15:774-779.
14. Forsberg, H., and Ljungdahl, P. O. 2001. Sensors of extracellular nutrients in Saccharomyces cerevisiae. Curr. Genet. 40:91-109.
15. Gold, S. E., Brogdon, S. M., Mayorga, M. E., and Kronstad, J. W. 1997. The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. Plant Cell 9:1585-1594.
16. Javelle, A., Morel, M., Rodriguez-Pastrana, B. R., Botton, B., Andre, B., Marini, A. M., Brun, A., and Chalot, M. 2003. Molecular characterization, function and regulation of ammonium transporters (Amt) and ammonium-metabolizing enzymes (GS, NADP-GDH) in the ectomycorrhizal fungus Hebeloma cylindrosporum. Mol. Microbiol. 47:411-430.
17. Javelle, A., Thomas, G., Marini, A. M., Krämer, R., and Merrick, M. 2005. In vivo functional characterization of the Escherichia coli ammonium channel AmtB: Evidence for metabolic coupling of AmtB to glutamine synthetase. Biochem. J. 390:215-222.
18. Kamaruddin, N., Bakar, F. A., Mahadi, N. M., and Murad, A. M. A. 2008. Isolation and characterization of a gene encoding the Colletotrichum gloeosporioides regulatory subunits for protein kinase A. J. Biol. Sci. 8:730-737.
19. Kojima, K., Kikuchi, T., Takano, Y., Oshiro, E., and Okuno, T. 2002. The mitogen-activated protein kinase gene MAF1 is essential for the early differentiation phase of appressorium formation in Colletotrichum lagenarium. Mol. Plant-Microbe Interact. 15:1268-1276.
20. Kramer-Haimovich, H., Servi, E., Katan, T., Rollins, J., Okon, Y., and Prusky, D. 2006. Effect of ammonia production by Colletotrichum gloeosporioides on pelB activation, pectate lyase secretion, and fruit pathogenicity. Appl. Environ. Microbiol. 72:1034-1039.
21. Kronstad, J. W. 1997. Virulence and cAMP in smuts, blasts and blights. Trends Plant Sci. 2:193-199.
22. Lee, N., D'Souza, C. A., and Kronstad, J. W. 2003. Of smuts, blasts, mildews, and blights: cAMP signaling in phytopathogenic fungi. Annu. Rev. Phytopathol. 41:399-427.
23. Lee, Y. H., and Dean, R. A. 1993. cAMP regulates infection structure formation in the plant pathogenic fungus Magnaporthe grisea. Plant Cell 5:693-700.
24. Lee, Y. H., and Dean, R. A. 1994. Hydrophobicity of contact surface induces appressorium formation in Magnaporthe grisea. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 115:71-75.
25. Lengeler, K. B., Davidson, R. C., D'Souza, C., Harashima, T., Shen, W. C., Wang, P., Pan, X., Waugh, M., and Heitman, J. 2000. Signal transduction cascades regulating fungal development and virulence. Mol. Microbiol. Biol. Rev. 64:746-785.
26. Liebmann, B., Müller, M., Braun, A., and Brakhage, A. A. 2004. The cyclic AMP-dependent protein kinase A network regulates development and virulence in Aspergillus fumigatus. Infect. Immun. 72:5193-5203.
27. Lorenz, M. C., and Heitman, J. 1998. The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO (Eur. Mol. Biol. Organ.) J. 17:1236-1247.
28. Magasanik, B. 2005. The transduction of the nitrogen regulation signal in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 102:16537-16538.
29. Manteau, S., Abouna, S., Lambert, B., and Legendre, L. 2003. Differential regulation by ambient pH of putative virulence factors secretion by the phytopathogenic fungus Botrytis cinerea. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol. 43:359-366.
30. Marini, A. M., Soussi-Boudekou, S., Vissers, S., and Andre, B. 1997. A family of ammonium transporters in Saccharomyces cerevisiae. Mol. Cell Biol. 17:4282-4293.
31. Mitchell, T. K., and Dean, R. A. 1995. The cAMP-dependent proteinkinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7:1869-1878.
32. Miyara, I., Shafran, H., Davidzon, M., Sherman, A., and Prusky, D. 2010. pH regulation of ammonia secretion by Colletotrichum gloeosporioides and its effect on appressorium formation and pathogenicity. Mol. Plant-Microbe Interact. 23:304-316.
33. Miyara, I., Shnaiderman, C., Meng, X., Vargas, W. A., Diaz-Minguez, J. M., Sherman, A., Thon, M., and Prusky, D. 2012. Role of nitrogenmetabolism genes expressed during pathogenicity of the alkalinizing Colletotrichum gloeosporioides and their differential expression in acidifying pathogens. Mol. Plant-Microbe Interact. 25:1251-1263.
34. Monahan, B. J., Askin, M. C., Hynes, M. J., and Davis, M. A. 2006. Differential expression of Aspergillus nidulans ammonium permease genes is regulated by GATA transcription factor AreA. Eukaryot. Cell 5:226-237.
35. O'Connell, R., Thon, M. R., Hacquard, S., Van Themaat, E. V. L., Amyotte, S. G., Kleemann, J., Torres, M. F., Damm, U., Buiate, E. A., Epstein, L., Alkan, N., Altmüller, J., Alvarado-Balderrama, L., Bauser, C. L., Becker, C., Birren, B. W., Chen, Z., Choi, J., Crouch, J. A., Duvick, J. P., Farman, M. L., Gan, P., Heiman, D., Henrissat, B., Howard, R. J., Kabbage, M., Koch, C., Kubo, Y., Law, A. D., Lebrun, M. H., Lee, Y. H., Miyara, I., Moore, N., Neumann, U., Panaccione, D. G., Panstruga, R., Place, M., Proctor, R. H., Prusky, D., Rech, G., Reinhardt, R., Rollins, J. A., Rounsley, S., Schard, C. L., Schwartz, D. C., Shenoy, N., Shirasu, K., Sikhakolli, U. R., Stüber, K., Sukno, S. A., Sweigard, J. A., Takano, Y., Takahara, H., Trail, F., Van der Does, H. C., Voll, L. M., Will, I., Young, S., Zeng, Q., Zhang, J., Zhou, S., Dickman, M. B., Schulze-Lefert, P., M. L. J., and Vaillancourt, L. J. 2012. Life-style transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat. Genet. 44:1060-1065
36. Oh, Y., Donofrio, N., Pan, H., Coughlan, S., Brown, D., Meng, S., Mitchell, T., and Dean, R. A. 2008. Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae. Genome Biol. 9:R85.
37. Prusky, D., and Yakoby, N. 2003. Pathogenic fungi: Leading or led by ambient pH? Mol. Plant Pathol. 4:509-516.
38. Prusky, D., McEvoy, J. L., Leverentz, B., and Conway, W. S. 2001. Local modulation of host pH by Colletotrichum species as a mechanism to increase virulence. Mol. Plant-Microbe Interact. 14:1105-1113.
39. Prusky, D., McEvoy, J. L., Saftner, R., Conway, W. S., and Jones, R. 2004. The relationship between host acidification and virulence of Penicillium spp. on apple and citrus fruit. Phytopathology 94:44-51.
40. Rohde, J. R., and Cardenas, M. E. 2004. Nutrient signaling through TOR kinases controls gene expression and cellular differentiation in fungi. Curr. Top. Microbiol. Immunol. 27:953-972.
41. Rollins, J. A., and Dickman, M. B. 2001. pH signaling in Sclerotinia sclerotiorum: Identification of pacC/RIM1 homolog. Appl. Environ. Microbiol. 67:75-81.
42. Shafran, H., Miyara, I., Eshed, R., Prusky, D., and Sherman, S. 2008. Development of new tools for studying gene function in fungi based on the Gateway system. Fungal Genet. Biol. 45:1147-1154.
43. Smith, D. G., Garcia-Pedrajas, M. D., Gold, S. E., and Perlin, M. H. 2003. Isolation and characterization from pathogenic fungi of genes encoding ammonium permeases and their roles in dimorphism. Mol. Microbiol. 50:259-275.
44. Soupene, E., He, L., Yan, D., and Kustu, S. 1998. Ammonia acquisition in enteric bacteria: Physiological role of the ammonium/methylammonium transport B (AmtB) protein. Proc. Natl. Acad. Sci. U. S. A. 95:7030-7034.
45. Soupene, E., Lee, H., and Kustu, S. 2002. Ammonium/methylammonium transport (Amt) proteins facilitate diffusion of NH3 bidirectionally. Proc. Natl. Acad. Sci. U. S. A. 99:3926-3931.
46. Stephenson, S. A., Green, J. R., Manners, J. M., and Maclean, D. J. 1997. Cloning and characterisation of glutamine synthetase from Colletotrichum gloeosporioides and demonstration of elevated expression during pathogenesis on Stylosanthes guianensis. Curr. Genet. 31:447-454.
47. Takano, Y., Kikuchi, T., Kubo, Y., Hamer, J. E., Mise, K., and Furusawa, I. 2000. The Colletotrichum lagenarium Map kinase gene CMK1 regulates diverse aspects of fungal pathogenesis. Mol. Plant-Microbe Interact. 13:374-383.
48. Taylor, S. S., Buechler, J. A., and Yonemoto, W. 1990. cAMP-dependent protein kinase: Framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59:971-1005.
49. Teichert, S., Rutherford, J. C., Wottawa, M., Heitman, J., and Tudzynski, B. 2008. Impact of ammonium permeases MepA, MepB, and MepC on nitrogen-regulated secondary metabolism in Fusarium fujikuroi. Eukaryot. Cell 2:187-201.
50. Tu, J. C. 1985. An improved Mathur's medium for growth, sporulation, and germination of spores of Colletotrichum lindemuthianum. Microbios 44:87-93.
51. Van Nuland, A., Vandormael, P., Donaton, M., Alenquer, M., Lourenco, A., Quintino, E., Versele, M., and Thevelein, J. M. 2006. Ammonium permease-based sensing mechanism for rapid ammonium activation of the protein kinase A pathway in yeast. Mol. Microbiol. 59:1485-1505.
52. Von Wiren, N., and Merrick, M. 2004. Regulation and function of ammonium carriers in bacteria, fungi and plants. Trends Curr. Genet. 9:95-120.
53. Xu, J. R. 2000. MAP kinases in fungal pathogens. Fungal Genet. Biol. 31:137-152.